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MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 458: 39–52, 2012
doi: 10.3354/meps09724
Published online July 3
OPEN
ACCESS
Tolerance of benthic macrofauna to hypoxia and
anoxia in shallow coastal seas: a realistic scenario
Bettina Riedel1,*, Martin Zuschin2, Michael Stachowitsch1
1
Department of Marine Biology and 2Department of Paleontology, University of Vienna, Althanstrasse 14, Vienna 1090, Austria
ABSTRACT: Oxygen depletion can lead to the collapse of benthic ecosystems, i.e. to dead zones,
and large-scale biodiversity loss. Based on mortality and survival, we evaluated ranges of sensitivity and tolerance to hypoxia levels, duration of anoxia and H2S exposure across taxa and key life
habits. Experiments were conducted on a sublittoral soft-bottom under realistic in situ conditions
in a community setting featuring both a well-developed epi- and infauna. Overall, 495 individuals
representing 40 species were examined over almost 1000 h (using time-lapse camera and sensor
arrays). Mortality started at dissolved oxygen (DO) concentrations < 0.5 ml l−1 and centred at the
transition from severe hypoxia to early anoxia. A total of 58% of the individuals belonging to 27
species died. Thirteen species (39 individuals) died exclusively during anoxia. All of the individuals that died during hypoxia, and most of those that died during anoxia, did so before the onset of
hydrogen sulphide (H2S). In 11 species, all individuals survived: survival rates were highest
among molluscs, anthozoans and ascidians. In contrast, most polychaetes, decapods and echinoderms died. Epifauna was more vulnerable than infauna, mobile forms were more vulnerable than
sessile forms, and predators more vulnerable than deposit-feeders and suspension-feeders. While
hypoxia primarily affected total abundance, anoxia significantly reduced the number of species.
The former represents a quantitative, the latter a qualitative decline in ecosystem function. Most
of the macrofauna may initially survive shorter-term (day-long) or intermittent hypoxia, but the
onset of anoxia marks community collapse and biodiversity loss.
KEY WORDS: Benthic community · Oxygen · Dead zone · Survival · Mortality · Life habit ·
Mediterranean
Resale or republication not permitted without written consent of the publisher
Many marine ecosystems have deteriorated to a
point that scientific publications increasingly focus
on ecosystem dysfunction (Jackson et al. 2001, Worm
et al. 2006, Jackson 2008) by documenting deterioration, identifying indicators and indices of habitat
quality and suggesting management strategies (Link
2005, Salas et al. 2006, Butchart et al. 2010). This is
most evident in shallow coastal seas, which bear the
brunt of virtually all anthropogenic disturbances
(Lotze et al. 2006, Halpern et al. 2008).
Among such threats, in particular eutrophicationpromoted hypoxia (dissolved oxygen [DO] < 2.0 ml l−1;
Diaz & Rosenberg 1995) and anoxia can depauperate
and ‘homogenise’ benthic communities or even eliminate the macrofauna entirely (Sala & Knowlton 2006).
This changes ecosystem structure and function (Gray
et al. 2002, Solan et al. 2004, Levin et al. 2009, Middelburg & Levin 2009) and leads to destabilisation
(Conley et al. 2009, Rabalais et al. 2010, Zhang et al.
2010). One endpoint is widespread ecosystem collapse. Accordingly, ecosystems suffering from intermittent or recurring hypoxia or anoxia are among the
most extreme marine environments based on both the
severity of conditions and the instability or unpredictability of disturbance. Global warming is expected to increase the vulnerability of benthic macrofauna
*Email: [email protected]
© Inter-Research 2012 · www.int-res.com
INTRODUCTION
40
Mar Ecol Prog Ser 458: 39–52, 2012
to reduced oxygen levels (Vaquer-Sunyer & Duarte
2010) and thus accelerate biodiversity loss (Keeling et
al. 2010, Gruber 2011).
Much of the available information about the
impact on benthic systems comes from laboratory
experiments on individual species (e.g. Shimps et al.
2005, Long et al. 2008, Wang et al. 2010), from a
piecemeal fabric of in situ documentations (e.g. Stachowitsch 1984) and, increasingly, from syntheses
based on organisms from different communities,
laboratory and field studies and different geographic regions (e.g. Vaquer-Sunyer & Duarte 2008,
Farrell & Richards 2009). Our efforts are designed to
fortify one cornerstone of these approaches, namely,
to document the impact on the benthos within the
same benthic community, in the field, over the
entire course from the onset of hypoxia to mortality.
The in situ experimental design (Stachowitsch et al.
2007) yields a more holistic picture by concurrently
presenting individual- to community-level responses
from different perspectives (i.e. behavioural reactions, intra- and interspecific interactions and mortality sequences).
Here, we build upon traditionally accepted oxygen
thresholds and examine them in a community setting. We define sensitivity or tolerance based on the
sequence of mortality and on survival at various taxonomic levels in relation to hypoxia and duration of
anoxia. We also consider ‘life habits’, i.e. substrate
relationship, mobility and feeding type. The results,
combined with behavioural studies, will provide
information on the sensitivity and function of the
benthic compartment and will help to better interpret
post-hypoxia or anoxia community composition and
recovery potential.
MATERIALS AND METHODS
Study site and experimental design
The Northern Adriatic Sea (Mediterranean) is
among the ca. 400 dead zones recognized by Diaz &
Rosenberg (2008) and combines most features that
characterise coastal ecosystems sensitive to low oxygen events (e.g. semi-enclosed basin, shallow depth,
soft bottom, high productivity and stratification; Stachowitsch & Avcin 1988). This model system shows
classical symptoms of long-term anthropogenic
eutrophication (Justic 1987), including repeated mortalities (e.g. Fedra et al. 1976, Stachowitsch 1984,
Hrs-Brenko et al. 1994), and is especially interesting
in featuring both a well-developed infauna and
macroepifauna (Zuschin & Stachowitsch 2009). The
investigated community was named the OphiothrixReniera-Microcosmus (ORM) community by Fedra et
al. (1976) based on the 3 dominant genera (the brittle
star Ophiothrix quinquemaculata, the sponge Reniera spp. and the ascidian Microcosmus sulcatus).
Eleven deployments of a specially designed camera- and sensor-equipped benthic chamber were
made in September 2005 and August to October 2006
in a soft-bottom habitat (poorly sorted silty sand) in
24 m depth in the Gulf of Trieste, Northern Adriatic
Sea (45° 32’ 55.68’’ N, 13° 33’ 1.89’’ E). This position is
adjacent to the oceanographic buoy of the Marine
Biology Station Piran and is one of the few sites in the
Gulf unaffected by bottom fisheries, a key criterion
for physically intact benthos and secure equipment
deployment. Moreover, this site has not been affected by hypoxia for at least 5 yr before our experiments (V. Malacic pers. comm.), providing a biologically intact community including the larger epifaunal
multi-species clumps that characterise the Gulf of
Trieste (Fedra et al. 1976).
The underwater device was used to experimentally
induce small-scale anoxia and quantify macrobenthic responses (for a detailed description of the
method, see Stachowitsch et al. 2007). The design
involves the successive use of 2 interchangeable
bases of the same size (50 × 50 × 50 cm). Initially, the
‘open’ configuration (aluminium frame plus separate
instrument lid) was positioned for ca. 1 d above a
benthic assemblage to document macrofaunal behaviour during normoxia. Then, in a second step, the
‘closed’ configuration (plexiglass chamber plus lid)
was positioned over the same assemblage to document reactions to hypoxia and anoxia (ca. 3 to 4 d).
The plexiglass chamber, pressed ca. 4 cm into the
sediment, prevented water exchange with the surrounding environment. The lid housed a digital camera, 2 flashes, a datalogger and the microsensor array
for DO, H2S and temperature recording (Unisense®).
To detect potential stratification, DO was measured
at 2 different heights (2 and 20 cm above the sediment); the H2S sensor was positioned 2 cm above the
sediment. pH was measured at the beginning and
end of almost all deployments with a WTW TA 197pH sensor. Images were taken in 6 min intervals,
with the sensor values logged every minute. The
flashes never triggered any visible reaction in the
benthic invertebrates, either in the open or closed
configuration, and were thus not considered to have
caused stress or altered the course of events. The
courses of all deployments were very similar, but the
starting times and durations varied due to weather
Riedel et al.: Tolerance of macrozoobenthos to oxygen depletion
conditions, diving schedules and different enclosed
fauna. After each deployment, all enclosed organisms (living and dead) were collected and preserved
in a 4% formalin-seawater solution. We attribute all
mortalities to our experimental set-up: based on the
short timeframe of our experiments (days), we consider the natural mortality of the long-lived macrobenthos to be negligible compared to that induced by
the rapid oxygen declines. The deployments followed institutional guidelines (Univ. of Vienna, Austria; Marine Biology Station Piran, Slovenia).
Macrofauna data analysis
The 11 deployments covered a total surface area of
2.75 m2 and yielded data on a representative spectrum of taxa, life habits and behaviours (the latter will
be summarised elsewhere). Overall, 9953 images
were produced, encompassing a documentation time
of 995 h (hypoxia: 331.9 h, anoxia: 336.5 h). A total of
495 individuals were evaluated, representing 39 species and 1 species group (i.e. polychaetes, containing
those individuals that could not be identified more
precisely based on the photographs) (Appendix 1).
The species represented by only 1 or a few individuals
were evaluated in full, those by many individuals
selectively (e.g. based on individuals that were
continuously visible — after emergence in the case
of infauna — and recognisable). Time-lapse movies
(Adobe Premiere Pro CS4) combined the images for
quick viewing (sample 4 d film available at http://
phaidra.univie.ac.at/o:87923). Death was defined as
having occurred directly after the final activity was
observed; based on the authors’ long-term experience,
this time-point was typically unambiguous (e.g. collapse of soft-bodied forms and various combinations
of overturning, clear-cut body postures, discoloration).
Survivorship curves of individuals, species and higher
taxa and species’ life habits were depicted in relation
to hypoxia concentration (ml l−1) and anoxia duration.
Importantly, the separation into hypoxia (based on
DO concentration) and anoxia (duration) yielded a
more detailed and more interpretable sequence and
range of tolerances, whereby mortality was additionally examined in terms of H2S concentration (µM; at
time of mortality during anoxia). Oxygen categories
are defined as normoxia (≥2.0 ml DO l−1), mild (< 2 ml
DO l−1, equivalent to 2.8 mg O2 l−1 or 91.4 mM; Diaz &
Rosenberg 1995), moderate (<1.0 ml DO l−1), or severe
hypoxia (< 0.5 ml DO l−1) and anoxia. Significant H2S
refers to concentrations >14 µM, as defined by Vaquer-Sunyer & Duarte (2010). Life habits include sub-
41
strate relationship (cryptic and non-cryptic epifauna
or infauna), mobility (mobile or sessile) and 3 major
feeding types (predators, suspension feeders or deposit feeders) (Appendix 1).
One-way repeated measures ANOVA was used to
test, across deployments, the equality of means of
abundance (individual, species and higher taxa) and
species’ life habits among key oxygen categories.
Within-subject comparisons that violated the assumption of sphericity were Greenhouse-Geisser corrected. Bonferroni-adjusted pairwise comparisons were
then used to further explore significant differences
(p < 0.05). Analyses were performed using the SPSS
19.0 software package.
RESULTS
Deployments
During the open configuration, the DO concentration remained relatively constant within a particular
deployment, ranging from 2.6 to 5.6 ml l−1 on the
bottom and from 2.8 to 8.9 ml l−1 20 cm above the
sediment. After closing the chamber, oxygen values
immediately fell, with both curves continuously approximating each other. This drop in oxygen solely reflects natural respiration rates: the light conditions at
this depth are low, our experiment never contained
macroalgae, and any photosynthesis by the microflora
is apparently negligible (based on the rapid decline of
oxygen) compared to the respiration rates of the enclosed fauna. Hypoxia was reached within ca. 1.5 d
and anoxia within 3 d (Table 1). The rapidity of the
oxygen decline varied among deployments, with the
duration of hypoxia ranging from 11.4 to 52.9 h and
5.2 to 81.8 h for anoxia. H2S developed in 10 deployments and started to increase soon after the onset of
anoxia, with final values reaching ~163.6 µM (except
deployment 11, with an intermediate peak of 300 µM).
The course of a representative deployment, based on
average values from Table 1, is presented in Fig. 1.
The temperature within a particular deployment remained constant (17.6 to 21.4°C; Table 1); the bottom
water salinity was 38 ‰. The bottom water pH
dropped from initially 8.2 to a minimum of 7.5.
Mortality
Overall, 299 of 495 individuals died (60%). These
included representatives of 27 of the 40 species evaluated. During hypoxia, 135 individuals (14 species)
Mar Ecol Prog Ser 458: 39–52, 2012
42
Table 1. Deployment overview. No.: number of deployment; OC: open configuration (frame); CC: closed configuration
(chamber); WW: wet weight; –: no data
No.
Date
(d.mo.yr)
1
17−22.09.05
2
24−27.09.05
3 27.09−01.10.05
4
05−08.08.06
5
17−21.09.06
6
21−24.09.06
7
25−29.09.06
8 29.09−02.10.06
9
05−10.10.06
10
10−14.10.06
11
17−21.10.06
Duration deployment
OC
CC
(h)
(h)
–
–
–
22.4
20.9
21.7
21.9
22.7
23.6
25.4
–
132.8
69.4
101.6
48.3
72.1
41.9
73
40.3
95.4
75.2
94.6
Duration CC
Hypoxia Anoxia
(h)
(h)
20.1
46.1
41.6
12.5
33.8
22.7
40.5
16.7
11.4
33.6
52.9
81.8
5.2
28.8
22.9
28.7
8.5
19.1
13.9
78.3
24.2
25.1
H2S (µM)
(average over
last hour)
Final
pH
167.6
5.5
36.8
5.2
124.2
0.0
19.3
11.8
106.7
18.2
124.5
–
–
–
7.9
7.7
–
7.8
7.9
7.5
7.8
7.8
died (Fig. 2A). The most sensitive species was the
bivalve Chlamys varia, with 1 juvenile dying at
moderate hypoxia (0.8 ml DO l−1) and a second at
severe hypoxia (0.5 ml DO l−1). The second most sensitive species were a group of decapods which died
at concentrations ranging from 0.4 to 0.03 ml DO l−1
(for details on median and range values, see Table S1
in the supplement at www.int-res.com/articles/
suppl/m458p039_supp.pdf). Two of these species, the
spider crab Eurynome aspera and cryptic Galathea
spp., died during severe hypoxia (E. aspera: 0.2 ml
DO l−1, Galathea spp.: 0.3 and 0.03 ml DO l−1), whereas the decorator crab Ethusa mascarone, the spider
crab Macropodia spp. and the pistol shrimp Alpheus
glaber survived the first 8 h of anoxia. The decapods
were followed by the sea urchins Psammechinus
TempeTotal
rature
biomass
(°C)
(g WW 0.25 m−2)
18.5
17.8
17.6
18.8
19.7
20.4
20.6
21.4
21.3
21.3
20.4
436.7
682.1
604.7
–
839.8
526.3
648.9
629.2
724.0
631.6
1042.7
DO concentration (ml l–1)
H2S concentration (µM)
microtuberculatus and Schizaster canaliferus, of
which the latter was the first infaunal species to
emerge from the sediment and die (median DO
0.09 ml l−1). This was followed by another echinoderm and a designating species of the community,
the brittle star Ophiothrix quinquemaculata; mortalities concentrated at the transition from hypoxia to
anoxia (hypoxia median DO 0.03 ml l−1, anoxia
median duration 6.1 h). More tolerant crustaceans
included the cryptic Pilumnus spinifer, 4 of 17 individuals died at hypoxia (median DO 0.02 ml l−1) and
12 died during anoxia (median duration 7.3 h).
Thirteen species (39 individuals) died exclusively
during anoxia (Fig. 2B). Among the most sensitive in
this group were the infauna brittle stars Amphiura
chiajei and Ophiura spp., with mortalities ranging
from 8.2 to 19.1 h of anoxia. More tol60
erant species included the infauna biClosed configuration (chamber)
5 Open frame
valves Venerupis cf. rhomboides and
Abra alba, with mortalities around
4
28 h, along with the holothurian
Normoxia
40
Ocnus planci (anoxia median duraOxygen
H2S
3
tion 23.3 h) and the first ascidian
species to die, Phallusia mammilata
2
(median 31.7 h). The most tolerant
mortality
20
decapods included the hermit crab
Mild
Paguristes eremita, with a median
1
Moderate hypoxia
lethal anoxia duration of 42.8 h, folAnoxia
Severe
lowed by the gastropod Hexaplex
0
0
trunculus (mortalities at h 46.3 and
1
12
21 1
12
24
36
48
60
72
51.5) and the sea anemone Calliactis
Deployment duration (h)
parasitica (median 52.5 h). Finally, at
Fig. 1. Representative sensor graph of all deployments (based on averaged
76.8 h of anoxia, 2 of the 10 investi−1
values in Table 1). The hypoxia threshold was 2 ml l dissolved oxygen (DO);
gated individuals of the ascidian
dashed lines (1 and 0.5 ml l−1 DO) separate different stages of hypoxia. Black
kiteshape schematically indicates onset and course of mortality
Microcosmus sulcatus died.
Species
0.8
D
0.8
A
0.4
0.4
0.2
0.2
Hypoxia (ml DO l–1)
0.6
0.6
0 0
0 0
E
B
20
20
Anoxia (h)
40
40
60
60
80 0
80 0
F
C
50
50
150
150
H2S (µM)
100
100
200
200
250
250
300
300
Fig. 2. (A,B,C) Species and (D,E,F) higher taxa mortality in relation to hypoxia (ml dissolved oxygen [DO] l−1) and anoxia duration (h). H2S concentrations: values at time
of mortality during anoxia. Box: interquartile range IQR, median indicated; whisker: top and bottom 25% of scores; s: score > 1.5 IQR; ✴: score > 3 IQR; ❚: single or simultaneous mortality. Arrangement of species and higher taxa according to median values and first mortality. M: Mollusca; A: Anthozoa; AS: Ascidiacea; P: Polychaeta;
D: Decapoda; E: Echinodermata. See Table S1 (in the supplement at www.int-res.com/articles/suppl/m458p039_supp.pdf) for detailed median and range values
Mollusca (M)
Decapoda (D)
Echinodermata (E)
Polychaeta (P)
Ascidiacea (AS)
Anthozoa (A)
Higher taxa
Microcosmus sulcatus (AS)
Calliactis parasitica (A)
Hexaplex trunculus (M)
Paguristes eremita (D)
Phallusia mammilata (AS)
Ocnus planci (E)
Abra alba (M)
Venerupis cf. rhomboides (M)
Ebalia tuberosa (D)
Glycera sp. (P)
Ophiura spp. (E)
Amphiura chiajei (E)
Inachus sp. (D)
Pilumnus spinifer (D)
Polychaeta indet. (P)
Diodora sp. (M)
Protula tubularia (P)
Ophiothrix quinquemaculata (E)
Pisidia longimana (D)
Schizaster canaliferus (E)
Psammechinus microtuberculatus (E)
Galathea sp. (D)
Alpheus glaber (D)
Eurynome aspera (D)
Macropodia spp. (D)
Ethusa mascarone (D)
Chlamys varia (M)
Riedel et al.: Tolerance of macrozoobenthos to oxygen depletion
43
Mar Ecol Prog Ser 458: 39–52, 2012
100
A
90
94
SD = 30.37
mean = 18.7
n = 299
No. of mortalities (ind.)
80
60
40
33
30
20
17
9
1
0
1
<0.8
0.6
7 7
4
0.4
0.2
<10
30
3 1 2
70
50
100
B
80
Survivors (%)
Fig. 2C depicts the respective H2S concentration
(min.: 0 µM, max.: 279 µM) at the time of mortality
during anoxia. Importantly, most species died before
H2S developed: 200 individuals (24 species) died during hypoxia or anoxia without sulphide, and 99 individuals (23 species) died during anoxia with sulphide
present. In general, species with the highest tolerance to anoxia also tolerated high H2S values
(Fig. 2C, top). Mortalities at values >163.6 µM all
reflect an intermittent H2S peak in one deployment,
explaining the high range of H2S values in Chlamys
varia (10.3 to 279 µM) and the serpulid tube worm
Protula tubularia (0 to 253 µM).
Higher taxa also showed a differentiated sequence
and range of mortalities (Fig. 2D–F). The mortalities
clearly centred in a narrow window between severe
hypoxia (median lethal DO of all taxa 0.09 ml l−1) and
early anoxia (overall median 7.6 h). Decapods were
the most sensitive, with mortalities concentrated
from 0.09 ml l−1 (median DO) to 4.5 h (median anoxia
duration), followed by echinoderms (0.07 ml l−1 for
12 h) and polychaetes (0.03 ml l−1 for 13.2 h; Fig. 2D).
More tolerant higher taxa, i.e. those dying during
anoxia only, included ascidians (median 38.7 h) and
anthozoans (median 52.5 h; Fig. 2E, top). The H2S
concentrations at the time of mortality (overall median 0.6 µM; Fig. 2F) reflect the tolerance to the duration of anoxia in Fig. 2E, i.e. the most tolerant species
are again ascidians and anthozoans (median H2S
63.0 to 109.9 µM). The wide plot for molluscs (but
mostly from 0.1 ml l−1 median DO to 24.5 h median
anoxia duration) reflects a wide range of tolerances
for the different species, intraspecific variances and a
few mortalities during the intermittent H2S peak in
one deployment.
species
60
individuals
40
20
Survivors/total number
Species: 24/40
Individuals: 196/495
0
0.6
<0.8
100
0.4
0.2
<10
30
50
70
M
A
C
80
Survivors (%)
44
AS
60
40
20
Survivors/total number
M: 123/136
A: 34/38
AS: 14/19
P: 2/20
D: 18/209
E: 5/73
P
D
E
0
Critical DO and anoxia ranges
Mortalities centred at the transition from severe
hypoxia to early anoxia, rapidly increasing from
9 individuals at < 0.3 ml to 30 at < 0.2 ml and 90 at
< 0.1 ml DO l−1 (Fig. 3A). The peak mortality was
reached within 10 h of anoxia (94 individuals), dropping by an additional 33 individuals within the next
10 h and 17 at 30 h. Note that the average H2S concentration across all 11 deployments within the first
10 h of anoxia was low, i.e. 9.3 µM. Accordingly, 229
of the 299 mortalities (77%) occurred before significant H2S development.
The results depict clear declines at the individual,
species and higher taxon level (Fig. 3B,C). The
overall number of species dropped from initially 40
0.4
<0.8
0.6
0.2 <10
Moderate Severe hypoxia
DO conc. (ml l–1)
30
50
Anoxia
70
Duration (h)
Fig. 3. (A) Number of individuals dying at hypoxia and
anoxia (n = 299). Survivorship curves of (B) species and individuals and (C) of higher taxa across hypoxia (ml dissolved
oxygen [DO] l−1) and duration of anoxia (h). Vertical line on
x-axis separates moderate and severe hypoxia. M: Mollusca;
A: Anthozoa; AS: Ascidiacea; P: Polychaeta; D: Decapoda;
E: Echinodermata
at normoxia to 38 under hypoxia and to 24 by the
end of the experiment, amounting to a total decrease in species abundance of 40% (see Table 2 in
the supplement). The corresponding decrease on
the individual level was from 495 to 362 at hypoxia
Riedel et al.: Tolerance of macrozoobenthos to oxygen depletion
to 196 at anoxia (overall decrease 61%). Survivorship curves (Fig. 3C) of higher taxa show a clear
separation into 2 groups, the first, with lower survival, comprising polychaetes (2 survivors out of
20 individuals), decapods (18 of 209) and echinoderms (5 of 73). Their mortality started much earlier
(during severe hypoxia) than in the second group,
and the steepest decline was at the transition from
hypoxia to anoxia. In contrast, the second group —
molluscs, anemones and ascidians — were only minimally reduced even after 80 h of anoxia (overall
decrease 10, 11 and 26%), and the decreases occurred primarily under anoxia (± 40 h). The 1-way
repeated measures ANOVA confirmed significant
effects of different oxygen conditions (normoxia, hypoxia and anoxia) on the mean abundance of individuals (F2, 20 = 17.9, p < 0.001), species (F1.24,12.42 =
19.79, p < 0.001) and higher taxa (F1.17,11.67 = 10.89,
p = 0.005). Pairwise comparisons of oxygen categories revealed significant differences for all taxonomic levels (p < 0.05); the one exception was for
higher taxa in the case of normoxia vs. hypoxia
(p = 0.5).
Fig. 4A,B shows the percentage of survivors and
mortalities within species and higher taxa (for
details on the ratio of dead and surviving individuals
per species, see also Appendix 1). In only 13
species, 11 of which are molluscs, did all individuals
survive. Importantly, based on individuals, 77% of
the survivors were represented by only 2 species
(the infaunal bivalve Corbula gibba and the sea
anemone Cereus pedunculatus). Survival was high
among molluscs (90%), anthozoans (90%) and
ascidians (74%) and low in polychaetes, echinoderms and decapods (10, 9 and 7%, respectively)
(Fig. 4B). The echinoderm survivors were 5 infaunal
sea urchins Schizaster canaliferus. In the decapods,
the survivors were 2 cryptic Nepinnotheres pinnotheres individuals, 13 of 22 hermit crabs Paguristes
eremita, 1 of 17 Pilumnus hirtellus and 2 of 3 Ebalia
tuberosa. Finally, in the polychaetes, 2 undetermined species survived.
45
at www.int-res.com/articles/suppl/m453p039_supp.
pdf) were especially vulnerable to decreasing oxygen concentrations (overall decrease 60%). In infauna, the overall decrease was 36%, with a major
drop during anoxia. Repeated measures ANOVAs
indicated significant impact of the 3 key oxygen
categories on both the epifauna (F1.31,13.14 = 18.33,
p < 0.001) and infauna (F1.32,13.19 = 9.13, p = 0.006).
While species abundance in both epi- and infauna
dropped significantly from normoxia to anoxia (pairwise comparison, p < 0.05), the decrease from hypoxia to anoxia was significant only for epifauna (for
all epifauna p = 0.007; cryptic epifauna: p = 0.001;
non-cryptic epifauna p = 0.027).
Sessile life-forms (Fig. 5B) were more tolerant
than mobile forms, with an overall decrease of
only 20% during late anoxia (> 40 h of anoxia).
The decrease in the number of mobile species was
twice as high (43%) and already started at severe
hypoxia; this corresponds to a drop in the mean
number of mobile species per deployment from 11
at normoxia to 9 under hypoxia to 5 during anoxia.
The impact of different oxygen categories was significant (repeated measures analyses F2, 20 = 21.52,
p < 0.001), and the paired comparisons showed
significant differences between normoxia and anoxia (p = 0.001) and between hypoxia and anoxia
(p = 0.005).
Predators were the first to react under severe
hypoxia (overall decrease 53%), followed by depositand suspension-feeding species (both decreasing
during anoxia by 64 and 67%, respectively) (Fig. 5C).
In all feeding types, decreasing oxygen concentrations significantly affected the mean species abundance of suspension feeders (F1.08,10.82 = 10.56, p =
0.007), deposit feeders (F2, 20 = 10.54, p = 0.001) and
predators (F2, 20 = 19.12, p < 0.001). The pairwise comparisons showed significant differences in all feeding
types between normoxia and anoxia (p < 0.05) as well
as between hypoxia and anoxia (with the exception
of deposit feeders, p = 0.072).
DISCUSSION
Life habits
Survivorship curves related to species’ substrate
relationship, mobility and feeding type showed clear
differences in sensitivity patterns (Fig. 5). Epifauna
(Fig. 5A) were affected earlier (severe hypoxia) and
more strongly than infauna (epifauna reduced from
initially 26 to 15 species; overall decrease 42%).
Cryptic epifauna (see Fig. S1 in the supplement
Quantifying ecosystem disturbance or dysfunction
is often difficult, even when the damage is visible
(e.g. benthic fisheries; Collie et al. 2000). Our in situ
approach provides a solid foundation for assessing
the response to anoxia as a major source of disturbance by examining mortality as the most clear-cut
symptom. Determining the sequence of mortalities
and differentiating between the more sensitive and
Mar Ecol Prog Ser 458: 39–52, 2012
46
A
Survival
Species
Mortality:
moderate hypoxia
severe hypoxia
anoxia
Tellina serrata (M) 1
Tellina ovata (M) 1
Dentalium sp. (M) 1
Nassarins cf. pygmaeus (M) 1
Capulus hungaricus (M) 1
Murex brandaris (M) 2
Parvicardium papillosum (M) 3
Fusinus rostratus (M) 4
Nucula nucleus (M) 8
Aporrhais pes-pelecani (M) 8
Corbula gibba (M) 66
Cereus pedunculatus (A) 28
Nepinnotheres pinnotheres (D) 2
Hexaplex trunculus (M) 24
Microcosmus sulcatus (AS) 10
Phallusia mammilata (AS) 9
Ebalia tuberosa (D) 3
Calliactis parasitica (A) 10
Paguristes eremita (D) 25
Diodora sp. (M) 5
Chlamys varia (M) 8
Schizaster canaliferus (E) 22
Polychaeta indet. (P) 17
Pilumnus spinifer (D) 17
Protula tubularia (P) 8
Alpheus glaber (D) 2
Ethusa mascarone (D) 2
Ophiothrix quinquemaculata (E) 26
Macropodia spp. (D) 7
Pisidia longimana (D) 150
Psammechinus microtuberculatus (E) 12
Eurynome aspera (D) 1
Galathea sp. (D) 2
Ocnus planci (E) 4
Ophiura spp. (E) 2
Amphiura chiajei (E) 7
Glycera sp. (P) 1
Inachus sp. (D) 1
Abra alba (M) 2
Venerupis cf. rhomboides (M) 1
0
20
40
60
80
100
80
100
Survival and mortality (%)
B
Higher taxa
Mollusca (M) 136
Anthozoa (A) 38
Ascidiacea (AS) 19
Polychaeta (P) 20
Decapoda (D) 209
Echinodermata (E) 73
0
20
40
60
Survival and mortality (%)
Fig. 4. Survival and mortality of (A) species and (B) higher taxa. Arrangement according to survivors (%) and mortality in
hypoxia or anoxia categories. M: Mollusca; A: Anthozoa; AS: Ascidiacea; P: Polychaeta; D: Decapoda; E: Echinodermata.
Number after abbreviation: number of individuals. Total number of individuals analysed: 495 (299 mortalities, 196 survivors;
for n, see also Appendix 1)
Riedel et al.: Tolerance of macrozoobenthos to oxygen depletion
more tolerant species (‘losers’ and ‘winners’; Roberts
& Brink 2010) provides a finer resolution and is also a
step forward in interpreting post-disturbance community compositions.
100
A
80
Substrate relationship
Infauna
60
Epifauna
40
20
Survivors/total number
Epifauna: 15/26
Infauna: 9/14
0
<0.8
0.6
0.4
0.2
<10
30
50
70
100
Surviving species (%)
B
80
Sessile
Mobility
Mobile
60
40
20
Survivors/total number
Sessile: 4/5
Mobile: 20/35
0
<0.8
0.6
0.4
0.2
<10
30
50
70
100
C
80
Feeding type
SF
60
D
P
40
20
Survivors/total number
Suspension feeder (SF): 8/12
Deposit feeder (D): 7/11
Predator (P): 9/17
0
<0.8
0.6
0.4
0.2
<10
Moderate Severe hypoxia
DO conc. (ml l–1)
30
50
70
Anoxia
Duration (h)
Fig. 5. Survivorship curves of species’ life habits across
hypoxia (ml dissolved oxygen [DO] l−1) and duration of
anoxia (h). Vertical line on x-axis separates moderate and
severe hypoxia
47
Mortality and survival
The experiments successfully mimicked the conditions and mortalities observed during earlier mortality events (Stachowitsch 1984). There was a clear
sequence in mortality, with decapods, echinoderms
and polychaetes showing lower tolerance and ascidians and anthozoans showing distinctly higher tolerance (Fig. 2D,E). While this broadly confirms previous studies (e.g. Diaz & Rosenberg 1995), the
results also present a more nuanced picture by highlighting inter- and intraspecific variability. Molluscs,
for example, are generally considered to be more
tolerant (in part reflecting metabolic adaptations, e.g.
Larade & Storey 2002). In our study, 13 of the total of
24 species with surviving representatives were molluscs (6 bivalves and 7 gastropods; Fig. 4). At the
same time, some molluscs were among the least tolerant, with individuals of mainly 2 species (Chlamys
varia and Diodora sp.) exhibiting early mortalities.
This level of detail of mortality extends earlier field
observations (e.g. Stachowitsch 1984, Jorgensen
1980) as well as recent reviews (e.g. Levin et al. 2009)
and meta-analyses (e.g. Vaquer-Sunyer & Duarte
2008). The earlier field observations of Stachowitsch
(1984) were not accompanied by any oxygen measurements. Moreover, the rapidity of the 1983 event
and the limits of the diving approach (1 data collection effort per day at 25 m depth) led to a very coarse
resolution of events and a restriction to the most
conspicuous species. This new level of resolution on
mortalities in the field includes numerous species
whose tolerance is very poorly described, such as
Phallusia mammilata (Fiala-Medioni 1979) and pea
crabs (Stauber 1945). It also contributes significantly
to the knowledge of representative soft-bottom
groups, including echinoderms (e.g. Psammechinus)
and molluscs such as Vetigastropoda (Diodora), Littorinimorpha (Capulus and Aporrhais), Neogastropoda
(Fusinus, Hexaplex and Murex), Protobranchia
(Nucula), Heterodonta (Parvicardium, Tellina and
Timoclea) and scaphopods (Dentalium). Finally, the
present study reports species that have rarely been
observed in situ (e.g. Alpheus glaber; P. Dworschak
pers. comm.).
Our data suggest that most of the macrobenthic
invertebrates survive short-term oxygen limitation
(1 to 2 d, approximately corresponding to the first
half of our closed-chamber experiments) and can
therefore tolerate intermittent periods of mild to
moderate hypoxia (> 0.5 ml DO l−1). Severe hypoxia
or anoxia, however, marks the critical threshold that
compromises ecological integrity. Accordingly, mor-
48
Mar Ecol Prog Ser 458: 39–52, 2012
tality started relatively late (< 0.5 ml DO l−1) and initially involved a significant drop in individual abundance. The main mortality peak was recorded at a
narrow hypoxia–anoxia range (Fig. 3). Subsequent
anoxia then considerably impacted the number of
species, which dropped by nearly half (40 to 24).
Importantly, most mortalities took place before significant H2S development. This in most cases allowed
a clear distinction of the roles of these 2 factors,
showing that oxygen conditions alone are sufficient
to cause quick and widespread community collapse.
The drop in pH from an initial 8.2 to average 7.8 by
the end of the deployments represents a considerable
change and resembles the predicted pH scenario for
the end of this century. Such a drop could significantly influence organisms’ fitness and survival (e.g.
Pörtner 2008), although we found no evidence in the
literature for the inhibition of organismic activities
over short exposure times, such as those in our
deployments. Nonetheless, those individuals dying
at late anoxia experienced high H2S concentrations
and low pH, a combination of stressors that could
affect survivorship more than any single factor alone.
Although our deployments do not specifically
address the length of exposure to hypoxia, this will
no doubt play a role in systems with prolonged
hypoxia. In the case of Pisidia longimana and Pilumnus spinifer, for example, mortalities occurred at
somewhat higher oxygen concentrations (i.e. earlier)
when oxygen decline was slower than when the
declines were rapid (e.g. P. longimana, slow decline:
lethal DO 0.17 ± 0.15 ml l−1, steep decline: 0.06 ±
0.07 ml l−1; Haselmair et al. 2010). Nonetheless, both
values were close together at the lower end of severe
hypoxia and probably would not be altered significantly by a considerably shorter or longer hypoxic
period. Importantly, we would also expect the interspecific succession of mortalities to remain the same
regardless of hypoxia duration. Finally, the rapidity
of the oxygen declines that we induced corresponds
well with the course of past anoxia events in the
Northern Adriatic: in the 1983 mass mortality event,
overall macrofauna biomass dropped quickly by
20% (Day 1) to 57% (Day 2) and finally 80 and 92%
(Days 3 and 4, respectively) (Stachowitsch 1986). Our
rapid oxygen declines therefore accurately mimicked
the speed of events in ‘natural’ anoxia events here.
The time-lapse images support the notion that the
habitat complexity created by 3-dimensional biotic
community structure can both accelerate mortalities
(e.g. sponge associates) and provide important refuges (elevated structures for mobile species to climb
up). Note, however, that almost all species showed
stress behaviour much earlier, i.e. at mild hypoxia
(Riedel et al. 2008a, Haselmair et al. 2010, Pretterebner et al. 2012). Clearly, the community setting and
sub-lethal responses must be considered when analysing overall hypoxia-induced impacts.
Life habits
Incorporating life habits promotes a process-oriented interpretation of ecosystem status. In the 3 key
life habit categories (substrate relationship, mobility
and feeding type), significant drops occurred in both
individuals and species. For a particular ecosystem
function, we interpret the individual loss within a
taxon as a quantitative decrease in function, whereas
the loss of the taxon as a whole is a qualitative
decrease in function. The suspension-feeding capacity is a case in point. A particular species typically
filters a certain range of particle sizes (e.g. Ward &
Shumway 2004). When some individuals of that species die, then other individuals continue to feed on
that particle size, representing a quantitative loss of
function. When the species itself is lost, then that particle size range may no longer be filtered out. From
the view of the overall filter-feeding capacity, this
represents a qualitative change (e.g. altered spectrum of particle sizes filtered out by remaining species); a distinct functional compartment is lost.
The fact that suspension feeders showed the least
decline of all feeding types, however, does not imply
unimpaired ecosystem function. For example, the
service provided by benthic filter-feeding communities as a natural eutrophication control (Officer et al.
1982) may be compromised. Thus, the loss of the
brittle star Ophiothrix quinquemaculata (up to 250
individuals per m²; Fedra et al. 1976) but survival of
the ascidian Microcosmus sulcatus may represent a
major shift in the particle types and sizes removed
from the water because these 2 species filter distinct
sizes (Gili & Coma 1998). Sponges, a characteristic
group in this benthic community, filter the smallest
particles. Their early loss (Stachowitsch 1984) represents another ‘qualitative’ change in filter-feeding
capacity. Clearly, such quantitative and qualitative
losses begin even before the last individuals of the
particular compartment die (‘functional extinction’).
Our benthic chamber effectively reduced oxygen
but also cut off the food supply to suspension feeders.
Although we did not consider this aspect, the relative
tolerance of this group makes it unlikely that reduced
food supply significantly affected the timing or sequence of mortalities over the short experimental
Riedel et al.: Tolerance of macrozoobenthos to oxygen depletion
periods. This is supported by the finding (Ott & Fedra
1977) that the benthic community here functions as a
stabilizing compartment: energy reserves are accumulated by the large-sized, long-lived macrofauna
during times of abundant food and used in times of
reduced supply. Such a longer-term stabilizing role
of the benthos indicates a minimal impact of a few
days without food input from the water column.
Regarding substrate relationship and mobility,
infauna was more tolerant than epifauna, and sessile
organisms were more tolerant than mobile organisms
(Fig. 5). This confirms trends elsewhere. Vistisen &
Vismann (1997), for example, recorded a significantly higher tolerance to both hypoxia and sulphide of
the infauna brittle star Amphiura filiformis compared
to the epibenthic brittle star Ophiura albida, while
Sagasti et al. (2001) reported trends of decreasing tolerance of mobile species relative to sessile species.
Infauna is typically better adapted to oxygen limitation in the upper sediment layer than epifauna, and
the fauna from environments that are low in oxygen
tend to be more tolerant of low oxygen conditions
(for general physiological adaption strategies, see
Burnett 1997 and Hagerman 1998). Finally, we argue
that many sessile forms might have developed a
higher tolerance level for adverse environmental conditions than mobile forms (which can flee). Although
our approach did not permit animals to escape from
the chamber, it did accommodate almost all species.
For example, emerging irregular sea urchins typically
moved only a short distance across the sediment before dying, only rarely touching a chamber wall. The
more mobile hermit crabs (Pretterebner et al. 2012)
and epifaunal brittle stars (Riedel et al. 2008a,b)
sought temporary refuge mostly on directly adjoining,
elevated multi-species clumps. In anoxic events measuring tens to hundreds or even thousands of square
kilometres, the ability to travel somewhat further
would not affect the survival of any benthic invertebrate or small benthic fish (e.g. gobies); the extensive
and relatively uniform soft-bottom Northern Adriatic
shelf provides little refuge beyond the multi-species
clumps already enclosed in the chamber. There are
no immediately adjoining habitats that would provide
more elevated structures to climb onto or that would
represent a shallow-water refuge.
Variability
Despite clear overall patterns of tolerance, we
recorded high intraspecific variability. This drawnout loss of individuals supports our conclusion that
49
short-term hypoxia primarily involves quantitative
losses rather than fundamentally altered community
structure and function. On the taxonomic level, tolerance varies within a species (e.g. life stage; Breitburg
1992, Miller et al. 2002), among species and among
higher taxa. Physiological differences, beyond the
above-discussed relative mobility, substrate relationship (see also Vaquer-Sunyer & Duarte 2008) or feeding type, help determine tolerance and survival.
Finally, physical and biological community structure
can play a role, whereby the loss of 1 species can
trigger further species loss, reducing ecosystem stability (O’Gorman et al. 2011). In the study area, for
example, the aggregated structure of the epifauna in
multi-species clumps may accelerate ecosystem collapse in a positive feedback loop (e.g. emergence
and death of cryptic species inhabiting sponges that
have died).
The hermit crab Paguristes eremita is an example
of a broad intraspecific variability (mortalities after
20 to 60 h of anoxia). Here, the range may be explained by variations in hermit crab size and weight,
the ability to seek temporary refuge (with or without
a shell) on top of multi-species clumps and by the
degree of H2S exposure (Pretterebner et al. 2012).
Such variability provides an evolutionary advantage
by buffering the population against stochastic,
extreme events (e.g. Denny et al. 2011).
The decapods also provide an example for interspecific variability. In general, they are considered
among the most vulnerable organisms (Diaz & Rosenberg 1995, Vaquer-Sunyer & Duarte 2008). Here,
mortalities began at a DO concentration of 0.4 ml l−1
in the decorator crab Ethusa mascarone. At the other
end of the spectrum, individual hermit crabs showed
a high tolerance to extended anoxia (median 42.8 h)
and high H2S (median 135 µM). The most resistant
decapods were the pea crab Nepinnotheres pinnotheres (survival: 90 h of hypoxia and anoxia, maximum H2S concentration 126 µM; Haselmair et al.
2010), probably reflecting their life habits in the gill
cavity of bivalves or ascidians.
In higher groups, the tolerance range of echinoderms (relatively sensitive), for example, differed
dramatically from that of the most tolerant group
(anthozoans). In the latter case, the tolerance reflects
a combination of behavioural reactions and physiological adaptations (i.e. stretched and raised tentacle
crowns or switching to anaerobic metabolism; Shick
1991, Riedel et al. 2008b).
Finally, our results address the current discussion
about whether traditional thresholds, if interpreted
and applied rigidly, adequately address the above-
Mar Ecol Prog Ser 458: 39–52, 2012
50
outlined variability (Richards 2011). We argue against
a strict interpretation of thresholds gained from experiments designed to reduce the environment to 1 or
2 parameters (oxygen and H2S concentration). Overall, the factors — the presence of additional stressors
(Vaquer-Sunyer & Duarte 2010), different inherent
tolerances of organisms, structural habitat conditions
(Godbold et al. 2011) that can increase or decrease
survival, behavioural responses such as aggregation
on elevated structures and interactions between such
aggregated organisms, and susceptibility to predators — represent difficult-to-predict and potentially
confounding influences on the effects of hypoxia on
benthic communities. Nonetheless, they can influence survival in many ways and should be considered, together, in realistic assessments.
Clearly, the survival of tolerant species (‘winners’
sensu Roberts & Brink 2010) does not make a ‘winning’ community. Approaches that incorporate the
full range of benthic reactions, from initial behavioural responses to mortalities and surviving species,
can go beyond gauging the current status of a community based on the immediate condition of the component species. Coupled with additional information
(e.g. on growth rates and immigration), these approaches can even be used to help reconstruct the
severity and timing of past disturbances based on the
composition and sizes of remaining species. Such
knowledge is a prerequisite for informed management decisions regarding species and ecosystem
protection.
Acknowledgements. The present study was financed by the
Austrian Science Fund (FWF; projects P17655-B03 and
P21542-B17). We thank C. Baranyi, J. Hohenegger and A.
Stargardt for help with data analysis and graphics and the
directors (V. Malacic and A. Malej) and staff at the Marine
Biology Station (MBS) Piran, Slovenia, for their great hospitality and support during the fieldwork. Finally, we thank 3
anonymous reviewers for their stimulating suggestions,
which we were happy to incorporate.
gia 629:21−29
➤ Denny MW, Wesley Dowd W, Bilir L, Mach KJ (2011)
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LITERATURE CITED
➤ Breitburg D (1992) Episodic hypoxia in Chesapeake Bay: ➤
➤
➤
➤
Interacting effects of recruitment, behavior, and physical
disturbance. Ecol Monogr 62:525−546
Burnett LE (1997) The challenge of living in hypoxic and
hypercapnic aquatic environments. Am Zool 37:633−640
Butchart SHM, Walpole M, Collen B, Van Strien A and
others (2010) Global biodiversity: indicators of recent
declines. Science 328:1164−1168
Collie JS, Hall SJ, Kaiser MJ, Poiner IR (2000) A quantitative
analysis of fishing impacts on shelf-sea benthos. J Anim
Ecol 69:785−798
Conley DJ, Carstensen J, Vaquer-Sunyer R, Duarte CM
(2009) Ecosystem thresholds with hypoxia. Hydrobiolo-
➤
➤
Spreading the risk: small-scale body temperature variation among intertidal organisms and its implications for
species persistence. J Exp Mar Biol Ecol 400:175−190
Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr Mar Biol Annu
Rev 33:245−303
Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926−929
Farrell AP, Richards JG (2009) Defining hypoxia: an integrative synthesis of the responses of fish to hypoxia. Fish
Physiol 27:487−503
Fedra K, Ölscher EM, Scherübel C, Stachowitsch M, Wurzian RS (1976) On the ecology of a North Adriatic benthic
community: distribution, standing crop and composition
of the macrobenthos. Mar Biol 38:129−145
Fiala-Medioni (1979) Effects of oxygen tension on pumping,
filtration and oxygen uptake in the ascidian Phallusia
mammilata. Mar Ecol Prog Ser 1:49−53
Gili JM, Coma R (1998) Benthic suspension feeders: their
paramount role in littoral marine food webs. Trends Ecol
Evol 13:316−321
Godbold JA, Bulling MT, Solan M (2011) Habitat structure
mediates biodiversity effects on ecosystem properties.
Proc R Soc Ser B Biol Sci 278:2510−2518
Gray JS, Wu RS, Or YY (2002) Effects of hypoxia and organic
enrichment on the coastal marine environment. Mar Ecol
Prog Ser 238:249−279
Gruber N (2011) Warming up, turning sour, losing breath:
ocean biogeochemistry under global change. Philos
Trans R Soc Lond A 369:1980−1996
Hagerman L (1998) Physiological flexibility; a necessity for
life in anoxic and sulphidic habitats. Hydrobiologia 375/
376:241−254
Halpern BS, Walbridge S, Selkoe KA, Kappel CV and others
(2008) A global map of human impact on marine ecosystems. Science 319:948−952
Haselmair A, Stachowitsch M, Zuschin M, Riedel B (2010)
Behaviour and mortality of benthic crustaceans in
response to experimentally induced hypoxia and anoxia
in situ. Mar Ecol Prog Ser 414:195−208
Hrs-Brenko M, Medakovic D, Labura Z, Zahtila E (1994)
Bivalve recovery after a mass mortality in the autumn of
1989 in the northern Adriatic Sea. Period Biol 96:455−458
Jackson JBC (2008) Ecological extinction and evolution in
the brave new ocean. Proc Natl Acad Sci USA 105:
11458−11465
Jackson JBC, Kirby MX, Berger WH, Bjorndal KA and others (2001) Historical overfishing and the recent collapse
of coastal ecosystems. Science 293:629−637
Jorgensen BB (1980) Seasonal oxygen depletion in the bottom waters of a Danish fjord and its effect on the benthic
community. Oikos 34:68−76
Justic D (1987) Long-term eutrophication of the northern
Adriatic Sea. Mar Pollut Bull 18:281−284
Keeling RF, Körtzinger A, Gruber N (2010) Ocean deoxygenation in a warming world. Annu Rev Mar Sci 2:
199−229
Larade K, Storey KB (2002) A profile of the metabolic responses to anoxia in marine invertebrates. In: Storey KB,
Storey JM (eds) Cell and molecular responses to stress.
Elsevier Press, Amsterdam, p 27–46
Levin LA, Ekau W, Gooday AJ, Jorissen F and others (2009)
Riedel et al.: Tolerance of macrozoobenthos to oxygen depletion
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
Effects of natural and human-induced hypoxia on coastal
benthos. Biogeosciences 6:2063−2098
Link JS (2005) Translating ecosystem indicators into decision criteria. ICES J Mar Sci 62:569−576
Long WC, Brylawski BJ, Seitz RD (2008) Behavioral effects
of low dissolved oxygen on the bivalve Macoma balthica.
J Exp Mar Biol Ecol 359:34−39
Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH and others
(2006) Depletion, degradation, and recovery potential of
estuaries and coastal seas. Science 312:1806−1809
Middelburg JJ, Levine LA (2009) Coastal hypoxia and sediment biogeochemistry. Biogeosciences 6:1273−1293
Miller DC, Poucher SL, Coiro L (2002) Determination of
lethal dissolved oxygen levels for selected marine and
estuarine fishes, crustaceans, and a bivalve. Mar Biol
140:287−296
O’Gorman EJ, Yearsley JM, Crowe TP, Emmerson MC,
Jacob U, Petchey OL (2011) Loss of functionally unique
species may gradually undermine ecosystems. Proc R
Soc Lond B 278:1886−1893
Officer CB, Smayda TJ, Mann R (1982) Benthic filter feeding: a natural eutrophication control. Mar Ecol Prog Ser
9:203−210
Ott J, Fedra K (1977) Stabilizing properties of a high-biomass benthic community in a fluctuating ecosystem.
Helgol Mar Res 30:485−494
Pörtner HO (2008) Ecosystem effects of ocean acidification
in times of ocean warming: a physiologists’s view. Mar
Ecol Prog Ser 373:203−217
Pretterebner K, Riedel B, Zuschin M, Stachowitsch M (2012)
Hermit crabs and their symbionts: reactions to artificially
induced anoxia on a sublittoral sediment bottom. J Exp
Mar Biol Ecol 10:23−33
Rabalais NN, Diaz RJ, Levin LA, Turner RE, Gilbert D,
Zhang J (2010) Dynamics and distribution of natural and
human-caused hypoxia. Biogeosciences 7:585−619
Richards JG (2011) Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J Exp Biol
214:191−199
Riedel B, Zuschin M, Haselmair A, Stachowitsch M (2008a)
Oxygen depletion under glass: behavioural responses of
benthic macrofauna to induced anoxia in the northern
Adriatic. J Exp Mar Biol Ecol 367:17−27
Riedel B, Stachowitsch M, Zuschin M (2008b) Sea anemones
and brittle stars: unexpected predatory interactions during induced in situ oxygen crises. Mar Biol 153:
1075−1085
Roberts SJ, Brink K (2010) Managing marine resources sustainably. Environment 52:44−52
Sagasti A, Schaffner LC, Duffy JE (2001) Effects of periodic
hypoxia on mortality, feeding and predation in an estuarine epifaunal community. J Exp Mar Biol Ecol 258:
257−283
Sala E, Knowlton N (2006) Global marine biodiversity
trends. Annu Rev Environ Resour 31:93−122
Salas F, Marcos C, Neto JM, Patricio J, Perez-Ruzafa A, Mar-
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
➤
51
ques JC (2006) User-friendly guide for using benthic ecological indicators in coastal and marine quality assessment. Ocean Coast Manag 49:308−331
Shick JM (1991) A functional biology of sea anemones.
Chapman & Hall, New York, NY
Shimps E, Rice JA, Osborne JA (2005) Hypoxia tolerance in
two juvenile estuary-dependent fishes. J Exp Mar Biol
Ecol 325:146−162
Solan M, Cardinale BJ, Downing AL, Engelhardt KAM, Ruesink JL, Srivastava DS (2004) Extinction and ecosystem
function in the marine benthos. Science 306:1177−1180
Stachowitsch M (1984) Mass mortality in the Gulf of Trieste:
the course of community destruction. PSZNI Mar Ecol 5:
243−264
Stachowitsch M (1986) The Gulf of Trieste: a sensitive
ecosystem. Nova Thalassia 8:221−235
Stachowitsch M, Avcin A (1988) Eutrophication-induced
modifications of benthic communities. In: Eutrophication
of the Mediterranean Sea: receiving capacity and monitoring of long-term effects, Vol 49. Unesco Technical
Reports in Marine Science, Bologna, p 67−80
Stachowitsch M, Riedel B, Zuschin M, Machan R (2007)
Oxygen depletion and benthic mortalities: the first in situ
experimental approach to documenting an elusive phenomenon. Limnol Oceanogr Methods 5:344−352
Stauber LA (1945) Pinnotheres ostreum, parasitic on the
American oyster, Ostrea (Gryphaea) virginica. Biol Bull
(Woods Hole) 88:269−291
Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia
for marine biodiversity. Proc Natl Acad Sci USA 105:
15452−15457
Vaquer-Sunyer R, Duarte CM (2010) Sulfide exposure accelerates hypoxia-driven mortality. Limnol Oceanogr 55:
1075−1082
Vaquer-Sunyer R, Duarte CM (2011) Temperature effects on
oxygen thresholds for hypoxia in marine benthic organisms. Glob Change Biol 17:1788–1797
Vistisen B, Vismann B (1997) Tolerance to low oxygen and
sulfide in Amphiura filiformis and Ophiura albida (Echinodermata: Ophiuroidea). Mar Biol 128:241−246
Wang Y, Hu M, Shin PKS, Cheung SG (2010) Induction of
anti-predator responses in the green-lipped mussel
Perna viridis under hypoxia. Mar Biol 157:747−754
Ward JE, Shumway SE (2004) Separating the grain from the
chaff: particle selection in suspension and deposit-feeding bivalves. J Exp Mar Biol Ecol 300:83−130
Worm B, Barbier EB, Beaumont N, Duffy JE and others
(2006) Impacts of biodiversity loss on ocean ecosystem
services. Science 314:787−790
Zhang J, Gilbert D, Gooday AJ, Levin L and others (2010)
Natural and human-induced hypoxia and consequences
for coastal areas: synthesis and future development. Biogeosciences 7:1443−1467
Zuschin M, Stachowitsch M (2009) Epifauna-dominated
benthic shelf assemblages: lessons from the modern
Adriatic Sea. Palaios 24:211−221
Mar Ecol Prog Ser 458: 39–52, 2012
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Appendix 1. Macrobenthic species (40 taxa) recorded. Higher taxa: Anthozoa, Mollusca, Polychaeta, Decapoda, Echinodermata, Ascidiacea. Life habits: epi, epifauna; cryp, cryptic; in, infauna; SF, suspension feeder; P, predator; D, deposit feeder.
na: not applicable
Higher taxa
Species
Abundance
Ratio
total
Living:Dead
Anthozoa
Calliactis parasitica
Cereus pedunculatus
Life
habits
Final, pre-mortality behaviour
10
28
6:4
28:0
epi, sessile, D
epi, sessile, SF
tentacle crown movement
na
8
1
5
4
24
1
2
8:0
1:0
2:3
4:0
22:2
1:0
2:0
in, mobile, D
epi, mobile, SF
epi, mobile, P
epi, mobile, P
epi, mobile, P
epi, mobile, P
epi, mobile, P
na
na
body movement (foot), locomotion
na
body movement (foot), locomotion
na
na
in, mobile, D
na
Mollusca
Gastropoda
Aporrhais pespelecani
Capulus hungaricus
Diodora sp.
Fusinus rostratus
Hexaplex trunculus
Nassarius cf. pygmaeus
Murex brandaris
Scaphopoda
Dentalium sp.
Bivalvia
Abra alba
Chlamys varia
Corbula gibba
Nucula nucleus
Parvicardium papillosum
Tellina serrata
Timoclea ovata
Venerupis cf. rhomboides
1
1:0
2
8
66
8
3
1
1
1
0:2
3:5
66:0
8:0
3:0
1:0
1:0
0:1
in, mobile, D
epi, mobile, SF
in, mobile, SF
in, mobile, D
in, mobile, SF
in, mobile, D
in, mobile, SF
in, mobile, SF
body movement (siphon)
sustained valve gap, mantle retraction
na
na
na
na
na
body movement (foot & siphon)
Polychaeta
indeterminate species
Glycera sp.
Protula tubularia
11
1
8
2:9
0:1
0:8
in, mobile, D/P
in, mobile, P
epi, sessile, SF
body movement
body movement
tentacle crown movement
2
3
2
1
2
1
7
2
22
17
150
0:2
2:1
0:2
0:1
0:2
0:1
0:7
2:0
13:9
1:16
0:150
epi, mobile, D
epi, mobile, P
epi/cryp, mobile, P
epi, mobile, P
epi/cryp, mobile, P
epi, mobile, P
epi, mobile, P
epi/cryp, mobile, P
epi, mobile, P
epi/cryp, mobile, P
epi/cryp, mobile, P
body movement (legs)
body movement (legs)
body movement (legs)
body movement (legs)
body movement (legs)
body movement (legs)
body movement (legs)
na
body movement, locomotion
body movement (legs)
body movement (legs)
0:4
epi, mobile, SF
tentacle crown movement
Decapoda
Alpheus glaber
Ebalia tuberosa
Ethusa mascarone
Eurynome aspera
Galathea spp.
Inachus sp.
Macropodia spp.
Nepinnotheres pinnotheres
Paguristes eremita
Pilumnus spinifer
Pisidia longimana
Echinodermata
Holothuroidea
Ocnus planci
4
Echinoidea
Psammechinus microtuberculatus 12
Schizaster canaliferus
22
Ophiuroidea
Ophiothrix quinquemaculata
26
Ophiura spp.
2
Amphiura chiajei
7
0:12
5:17
epi, mobile, D
in, mobile, D
locomotion
locomotion
0:26
0:2
0:7
epi, mobile, SF
inf, mobile, D
inf, mobile, D
body movement (arms)
body movement (arms), locomotion
body movement (arms), locomotion
Ascidiacea
Microcosmus sulcatus
Phallusia mammilata
8:2
6:3
epi, sessile, SF
epi, sessile, SF
body contraction
body contraction
Editorial responsibility: William Kemp,
Cambridge, Maryland, USA
10
9
Submitted: November 23, 2011; Accepted: March 14, 2012
Proofs received from author(s): June 18, 2012